α-Helices direct excitation energy flow in the Fenna–Matthews–Olson protein
- Frank Müh†,‡,
- Mohamed El-Amine Madjet†,
- Julia Adolphs†,
- Ayjamal Abdurahman†,§,
- Björn Rabenstein†,
- Hiroshi Ishikita†,¶,
- Ernst-Walter Knapp†, and
- Thomas Renger†,‡
- †Institute for Chemistry and Biochemistry (Crystallography), Free University of Berlin, Takustrasse 6, 14195 Berlin, Germany;
- §Department of Physics, Xinjiang University, Urumqi 830046, China; and
- ¶Department of Chemistry, University of Southern California, Los Angeles, CA 90089
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Communicated by Rudolph A. Marcus, California Institute of Technology, Pasadena, CA, August 30, 2007 (received for review April 13, 2007)
Abstract
In photosynthesis, light is captured by antenna proteins. These proteins transfer the excitation energy with almost 100% quantum efficiency to the reaction centers, where charge separation takes place. The time scale and pathways of this transfer are controlled by the protein scaffold, which holds the pigments at optimal geometry and tunes their excitation energies (site energies). The detailed understanding of the tuning of site energies by the protein has been an unsolved problem since the first high-resolution crystal structure of a light-harvesting antenna appeared >30 years ago [Fenna RE, Matthews BW (1975) Nature 258:573–577]. Here, we present a combined quantum chemical/electrostatic approach to compute site energies that considers the whole protein in atomic detail and provides the missing link between crystallography and spectroscopy. The calculation of site energies of the Fenna–Matthews–Olson protein results in optical spectra that are in quantitative agreement with experiment and reveals an unexpectedly strong influence of the backbone of two α-helices. The electric field from the latter defines the direction of excitation energy flow in the Fenna–Matthews–Olson protein, whereas the effects of amino acid side chains, hitherto thought to be crucial, largely compensate each other. This result challenges the current view of how energy flow is regulated in pigment–protein complexes and demonstrates that attention has to be paid to the backbone architecture.
Footnotes
- ‡To whom correspondence may be addressed. E-mail: mueh{at}chemie.fu-berlin.de or rth{at}chemie.fu-berlin.de
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Author contributions: T.R. designed research; F.M., M.E.M., J.A., A.A., and T.R. performed research; B.R., H.I., and E.-W.K. contributed new analytic tools; F.M. analyzed data; and F.M. and T.R. wrote the paper.
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The authors declare no conflict of interest.
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This article contains supporting information online at www.pnas.org/cgi/content/full/0708222104/DC1.
- Abbreviations:
- BChla,
- bacteriochlorophyll a;
- FMO,
- Fenna–Matthews–Olson protein;
- PPC,
- pigment–protein complex.
- © 2007 by The National Academy of Sciences of the USA
